Castro-Diez - Et - Al - 2017 - Effects of Non-Native Tree

Biol. Rev. (2019), pp. 000–000.
1
doi: 10.1111/brv.12511
Global effects of non-native tree species on

multiple ecosystem services
Pilar Castro-Díez1,∗ , Ana Sofia Vaz2,3 , Joaquim S. Silva4,5 , Marcela van Loo6 ,
Álvaro Alonso1 , Cristina Aponte7 , Álvaro Bayón8 , Peter J. Bellingham9 ,
Mariana C. Chiuffo10 , Nicole DiManno11 , Kahua Julian11 , Susanne Kandert12 ,
Nicola La Porta13,14 , Hélia Marchante4,15 , Hamish G. Maule9 , Margaret M. Mayfield16 ,
Daniel Metcalfe17 , M. Cristina Monteverdi18 , Martín A. Núñez10 , Rebecca Ostertag11 ,
Ingrid M. Parker19 , Duane A. Peltzer9 , Luke J. Potgieter20 , Maia Raymundo16 ,
Donald Rayome21 , Orna Reisman-Berman22 , David M. Richardson20 ,
Ruben E. Roos23 , Asunción Saldaña1 , Ross T. Shackleton20 , Agostina Torres10 ,
Melinda Trudgen24,25 , Josef Urban26,27 , Joana R. Vicente2,28 , Montserrat Vilà8 ,
Tiina Ylioja29 , Rafael D. Zenni30 and Oscar Godoy31
1
Departamento de Ciencias de la Vida, Facultad de Ciencias, Universidad de Alcalá, E-28805, Alcalá de Henares, Spain
2
Research Network in Biodiversity and Evolutionary Biology, Research Centre in Biodiversity and Genetic Resources (InBIO-CIBIO),
Universidade do Porto, PT4485-661, Vairão, Portugal
3
Faculdade de Ciências, Universidade do Porto, PT4169-007, Porto, Portugal
4
College of Agriculture, Polytechnic Institute of Coimbra, 3045-601, Coimbra, Portugal
5
Centre for Applied Ecology ‘‘Prof. Baeta Neves’’ (InBIO-CEABN), School of Agriculture, University of Lisbon, PT1349-017, Lisbon, Portugal
6
Department of Botany and Biodiversity Research, University of Vienna, 1030, Vienna, Austria
7
School of Ecosystem and Forest Sciences, Faculty of Science, The University of Melbourne, Richmond, Victoria 3121, Australia
8
Department of Integrative Ecology, Estación Biológica de Doñana (EBD-CSIC), E-41092, Sevilla, Spain
9 Landcare Research, Lincoln, 7640, New Zealand
10
Grupo de Ecología de Invasiones, INIBIOMA, Universidad Nacional del Comahue, CONICET, Avenida de los Pioneros 2350, San Carlos de
Bariloche, Río Negro, Argentina
11 Department of Biology, University of Hawai’i at Hilo, Hilo, HI 96720, U.S.A.
12
University of Göttingen, 37073, Göttingen, Germany
13
IASMA Research and Innovation Centre, Fondazione Edmund Mach, 38010, Trento, Italy
14 MOUNTFOR Project Centre, European Forest Institute, 38010, Trento, Italy
15
Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, 3000-456, Coimbra, Portugal
16
The University of Queensland, School of Biological Sciences, Brisbane, Queensland 4072, Australia
17
CSIRO Land and Water, Ecosciences Precinct, Dutton Park, Queensland 4102, Australia
18
CREA Research Centre for Foresty and Wood, Viale Santa Margherita, 80 52100, Arezzo, Italy
19
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, U.S.A.
20
Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Matieland, 7602, South Africa
21
USDA Forest Service, Institute of Pacific Islands Forestry, Hilo, HI U.S.A.
22
French Associates Institute for Agriculture and Biotechnology of Drylands. Blaustein Institutes for Desert Research, Ben Gurion University of the
Negev, Beersheba, 84990, Israel
23
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway
24 CSIRO Land & Water, Wembley, Western Australia 6913, Australia
25
School of Biological Sciences, University of Western Australia, Crawley, Western Australia 6009, Australia
26
Faculty of Forestry and Wood Technology, Mendel University in Brno, 613 00, Brno-sever, Czech Republic
27 Siberian Federal University, Krasnoyarsk, Krasnoyarsk, 660041, Russia
* Author for correspondence: (E-mail: Tel.: +34 91 8855091; mpilar.castro@uah.es).
Biological Reviews (2019) 000–000 © 2019 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided
the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
2 Pilar Castro-Díez and others
28
Laboratory of Applied Ecology, CITAB – Centre for the Research and Technology of Agro-Environment and Biological Sciences, University of
Trás-os-Montes e Alto Douro, Vila Real, Portugal
29
Natural Resources Institute Finland (Luke), FI-00791, Helsinki, Finland
30
Setor de Ecologia, Departamento de Biologia, Universidade Federal de Lavras, Lavras, MG 37200-000, Brazil
31
Departamento de Biología, Facultad de Cc. del Mar y Ambientales, Instituto Universitario de Investigación Marina (INMAR), Campus de
Excelencia Internacional del Mar CEIMAR, Universidad de Cádiz, E-11510, Puerto Real, Spain
ABSTRACT
Non-native tree (NNT) species have been transported worldwide to create or enhance services that are fundamental
for human well-being, such as timber provision, erosion control or ornamental value; yet NNTs can also produce
undesired effects, such as fire proneness or pollen allergenicity. Despite the variety of effects that NNTs have on multiple
ecosystem services, a global quantitative assessment of their costs and benefits is still lacking. Such information is critical
for decision-making, management and sustainable exploitation of NNTs. We present here a global assessment of NNT
effects on the three main categories of ecosystem services, including regulating (RES), provisioning (PES) and cultural
services (CES), and on an ecosystem disservice (EDS), i.e. pollen allergenicity. By searching the scientific literature,
country forestry reports, and social media, we compiled a global data set of 1683 case studies from over 125 NNT
species, covering 44 countries, all continents but Antarctica, and seven biomes. Using different meta-analysis techniques,
we found that, while NNTs increase most RES (e.g. climate regulation, soil erosion control, fertility and formation),
they decrease PES (e.g. NNTs contribute less than native trees to global timber provision). Also, they have different
effects on CES (e.g. increase aesthetic values but decrease scientific interest), and no effect on the EDS considered.
NNT effects on each ecosystem (dis)service showed a strong context dependency, varying across NNT types, biomes
and socio-economic conditions. For instance, some RES are increased more by NNTs able to fix atmospheric nitrogen,
and when the ecosystem is located in low-latitude biomes; some CES are increased more by NNTs in less-wealthy
countries or in countries with higher gross domestic products. The effects of NNTs on several ecosystem (dis)services
exhibited some synergies (e.g. among soil fertility, soil formation and climate regulation or between aesthetic values
and pollen allergenicity), but also trade-offs (e.g. between fire regulation and soil erosion control). Our analyses provide
a quantitative understanding of the complex synergies, trade-offs and context dependencies involved for the effects of
NNTs that is essential for attaining a sustained provision of ecosystem services.
Key words: biological invasions, cultural ecosystem services, exotic trees, forestry, global assessment, meta-analysis,
provisioning ecosystem services, regulating ecosystem services.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
II. Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
(1) Data compilation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(a) Regulating ecosystem services (RES) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(b) Provisioning ecosystem services (PES) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(c) Cultural ecosystem services (CES) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(d) Ecosystem disservice (EDS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(e) Predictors of the variation of NNT effects on ecosystem (dis) services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(2) Data analyses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(a) Computation of grand mean effect size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(b) Computation of heterogeneity and structured meta-analyses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
(c) Publication bias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
(d) Synergies and trade-offs between ecosystem (dis)services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
III. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
(1) Description of the data set . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
(2) Effects of non-native tree species on regulating ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
(3) Effects of non-native tree species on provisioning ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
(4) Effects of non-native tree species on cultural ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
(5) Effects of non-native tree species on the ecosystem disservice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
(6) Relationships between ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
IV. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
Non-native tree effects on ecosystem services 3
(1) The data set . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

(2) Effects of non-native trees on ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
(3) Variability of non-native tree effects on ecosystem services worldwide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
(4) Synergies and trade-offs among the effects of non-native trees on ecosystem services . . . . . . . . . . . . . . . . . 18
(5) Methodological limitations and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
VI. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
VII. Author contributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
VIII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
IX. Supporting Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
I. INTRODUCTION & Vilà, 2017; Schindler et al., 2015). These costs may be
exacerbated when NNTs naturalize, and especially if they
Humans rely on the multiple services that ecosystems provide become invasive by spreading outside the areas where they
(MEA, 2005). Tree species play a key role in delivering were planted (Brundu & Richardson, 2016; Richardson &
ecosystem services, as they provide products (i.e. provisioning Rejmánek, 2011). Understanding how NNTs affect multiple
services, PES) such as timber, firewood, fibre, pulp or fodder. (dis)services and how these effects correlate with each other
They also contribute to regulatory processes (regulating is essential for enabling policy makers to balance costs and
services, RES), such as climate regulation (via carbon uptake), benefits, and manage conflicts over the use of NNTs (Dickie
soil formation and stabilization, and nutrient and water et al., 2014a; Pejchar & Mooney, 2009).
cycling (MacDicken, 2015; MacDicken et al., 2015). Trees Most of our knowledge on the effects of NNTs on
also offer non-material benefits (cultural services, CES), such ecosystem services derives from local or regional studies, but
as aesthetic or inspiration values; they are featured in the these effects likely depend on the environmental conditions,
folklore, tales and legends of most human cultures, and history and cultural background of each region (Castro-Díez
contribute to people’s sense of place (Kueffer & Kull, 2017; et al., 2014a; Corbin & D’Antonio, 2011; Kueffer & Kull,
Mason et al., 2017). 2017). Moreover, current knowledge is biased towards
With the increasing global demands of tree-derived easy-to-study services and the most widely distributed NNTs
ecosystem services (MacDicken et al., 2015), many (Hernandez-Morcillo, Plieninger & Bieling, 2013; Hulme
fast-growing, stress-tolerant or simply beautiful tree species et al., 2013). Furthermore, many costs and benefits caused
have been extensively planted beyond their native ranges by NNTs are reported by different actors with multiple
(Brundu & Richardson, 2016; Dickie et al., 2014a; Evans, disciplinary backgrounds (e.g. foresters versus conservation
2009). Examples include non-native conifers being planted biologists) using distinct publication types (e.g. scientific
worldwide for timber and pulp (Brundu & Richardson, 2016); papers, reports or social media) (Krumm & Vítková, 2016).
Acacia, Eucalyptus or Pinus boosting land reclamation and This paper presents the first global assessment of NNT effects
sand dune stabilization worldwide (Evans, 2009; Griffin et al., on multiple ecosystem (dis)services, covering the three main
2011); legume trees (e.g. Acacia, Gleditsia or Prosopis) being used categories of ecosystem services: regulating, provisioning
to prevent desertification and provide fodder or firewood in and cultural services (de Bello et al., 2010; Haines-Young &
arid and impoverished regions of Africa and Asia (Shackleton Potschin, 2013; MEA, 2005), and an ecosystem disservice.
et al., 2014; Witt, 2017); and shade and ornamental trees (e.g. Specifically, we (i) evaluate the overall magnitude and
Ailanthus, Jacaranda, Prosopis, Platanus and Robinia) providing direction of the effects that NNTs have on multiple ecosystem
amenities to rural and urban populations worldwide (Dickie (dis)services, using native vegetation as a control; (ii) explore
et al., 2014a). Yet, many non-native tree (NNT) species the role of environmental, geographical and socio-economic
also contribute to landscape homogenization, reduce native factors as potential predictors of the variation of NNT effects
biodiversity, and alter ecosystem functioning in undesirable on (dis)services; and (iii) identify synergies and trade-offs
ways (Cardinale et al., 2012; Gaertner, Richardson & Privett, among NNT effects on different ecosystem (dis)services. We
2011; Gamfeldt et al., 2013). NNTs may even result in address these questions through a global meta-analysis of a
direct negative impacts on human well-being (i.e. ecosystem comprehensive data set gathered from published scientific
disservices, EDS) (Shackleton et al., 2016), such as toxicity or literature, country-level economic and forestry reports, and
allergenicity. Therefore, NNTs also create threats to people’s social media.
livelihoods and human well-being, such as depletion of soil
nutrients and water reserves (Castro-Díez et al., 2012; Le
Maitre et al., 1996; Shackleton et al., 2014), increased fire
hazard (D’Antonio, 2000; Gaertner, Le Maitre & Esler, II. MATERIALS AND METHODS
2017; Nagler et al., 2005), damage to infrastructure and
archaeological remains (Booy et al., 2017; Celesti-Grapow Given that different stakeholders may perceive the same
& Blasi, 2004), or harm to human health (Nentwig, Mebs service change as beneficial or detrimental, we avoid
the value-laden term ‘impact’ and use the more neutral each RES, we identified a set of underlying target variables
one ‘effect’ to document objectively the changes produced which covered ecosystem properties, processes, and/or traits
by NNTs on ecosystem (dis)services (Jeschke et al., 2014). of dominant species that underpin the capacity of ecosystems
Thus, although throughout the manuscript we describe an to regulate processes and mitigate effects of disturbances
effect as an increase/decrease of a (dis)service (Pyšek et al., (de Bello et al., 2010; Quetier et al., 2007) (Table 1). We
2012), we merely inform on the direction of the change, performed a literature search of scientific publications, using
rather than judging the value of the change. ISI Web of Knowledge (http://webofknowledge.com/) and
Scopus (https://www.scopus.com). The search was carried out
(1) Data compilation in December 2015 and updated in December 2016, covering
the period between 1904 and 2015 with no restriction on
We focused on NNTs worldwide. We defined trees language. Our search string included: (Exotic* OR Alien*
as ‘perennial woody plants with many secondary branches OR invas*) AND (*native*) AND (tree*) AND the set of key
supported clear of the ground on a single main stem or trunk words shown in Table 1 combined with ‘OR’.
with clear apical dominance (including palms)’ (Richardson Publications retrieved from our searches were filtered
& Rejmánek, 2011, p. 789). ‘Non-native’ trees were defined according to the following criteria: (i) the study compares
as tree species introduced (accidentally or intentionally) any target variable between a site dominated by a NNT
by humans to new geographic areas, considering the and a control site with native vegetation; (ii) the NNT site
whole introduction–naturalization–invasion continuum (i.e. and the control site are close to each other and have similar
planted, naturalized and invasive species) (Richardson, Pyšek environmental conditions, according to the authors of the
& Carlton, 2011). The ‘non-native’ status of a tree was stated papers; and (iii) the paper provides means, deviation and
at the species level (i.e. ignoring the distribution of subspecies sample size of the target variable. The final number of
or varieties) and at the country scale, following regional selected papers was 135 (Appendix S2).
and national floras and checklists (see online Supporting Using data obtained from the selected publications,
information, Appendix S1). For Brazil, USA and Canada individual data sets were created for each RES (see Table 1).
however, non-native status was considered at the state level Each data set consisted of a table where rows were case studies
due to their large size and environmental and biogeographic and columns covered the mean, deviation and replication of
heterogeneity. Archaeophytes (i.e. species introduced before a target variable in a NNT site and in a control site, as well as
1492) were excluded because in many cases they could not other explanatory variables, which were subsequently used
be clearly assigned to native tree (NT) or NNT at a country to explain the variability of effect sizes (see Section II.1e).
level. Hybrids between NTs and NNTs were also excluded When the same paper provided measures on more than one
for the same reason. target variable, we adopted any of the following decisions: (i)
We covered the three most widely recognized categories for variables associated with different ecosystem services, we
of ecosystem services (de Bello et al., 2010; Haines-Young kept them as independent case studies because each service
& Potschin, 2013; MEA, 2005), i.e. regulating (RES), was independently analysed; and (ii) for variables associated
provisioning (PES) and cultural (CES) ecosystem services. with the same service, we selected the one most directly
We also considered an ecosystem disservice (EDS) – i.e. related to the service or we aggregated all values into one
a negative impact on human well-being (Shackleton et al., to avoid pseudo-replication (see Appendix S3 for details). In
2016) – specifically pollen allergenicity, which can be total, our data set contained 1688 case studies.
treated as a potential drawback from NNTs to human For each case study we calculated a standardized effect
health (Vaz et al., 2017b). The selection of variables and size using Hedges’ d (Rosenberg, Adams & Gurevitch, 2000),
data sources for each ecosystem (dis)service was achieved i.e. the difference of mean values between the NNT and
through an international participatory approach under the the control site, weighted by the number of replications and
COST Action FP1403: Non-native tree species for European by the inverse of the variance (Appendix S4A). When the
forests – experiences, risks and opportunities (http://nnext.boku.ac variable had a negative relation with the ecosystem service,
.at), and relied on the possibility of worldwide coverage, cost we changed the sign of the effect size. A positive effect size
and time efficiency, availability, and ease of communication thus indicates that the NNT site has a higher contribution to
across multiple countries. Data for RES were derived from the particular ecosystem service than the control site and vice
an extensive scientific literature review, while data for PES, versa.
CES and EDS were collected from a thorough information
search on reports and websites, among other sources (see (b) Provisioning ecosystem services (PES)
Sections II.1a–d).
We considered two main categories of products obtained
from areas where land cover was classified as ‘forest’:
(a) Regulating ecosystem services (RES)
timber products (any kind of goods obtained from harvesting
We agreed on a list of 10 relevant RES that cover the benefits trees) and non-timber products (any biological resource
that people obtain from the capacity of ecosystems to regulate in woodland except timber) (MEA, 2005). Details on the types
climate, floods, disease, waste, and water (de Bello et al., of products included in each category and specific sources of
2010; Haines-Young & Potschin, 2013; MEA, 2005). For information for each country are shown in Appendix S5.
Table 1. Target variables used as proxies for different regulating ecosystem services (RES). Variables include quantifications of
ecosystem processes, ecosystem or community properties and traits of dominant plant species. The positive or negative sign beside
each variable indicates the relation with the ecosystem service. The last column shows the list of specific key words used in the search
in ISI Web of Knowledge and Scopus
Target variables
Regulating ecosystem Ecosystem/community Key words used in the
services Ecosystem processes properties Plant species traits literature search†
Climate regulation Carbon sequestration + Aboveground plant Chlorophyll concentration Carbon sequestration,
Biomass production+ mass/C + + Carbon storage,
Root mass + Photosynthetic rate + Primary production,
Soil carbon + Relative growth rate + RGR, Growth rate,
Total plant mass + Tree height + Photosynthetic rate,
Tree basal area + Trunk area/diameter + Chlorophyll
Trunk diameter concentration,
increment + Microclimate, Climate
regulation, Canopy
temperature, Wind
Fire-risk prevention Canopy fuel continuity – Calorific value – Fire, Fire frequency, Fire
Canopy water content + Effective heat of susceptibility, Fire
Litter mass/depth – combustion – intensity, Burning
Litter water content + Leaf moisture + temperature, Fire
Understorey biomass – Volatile compounds – spread, Forest fire,
Wildfire
Fire regime, Fire
behavio?r, Fuel
propert*, Flammability
Flood regulation Flood frequency – Flood frequency, Flood*
Stream water velocity – Water velocity, River
flow, Run?off, Flood
protection, Flood
defence, Flood storage,
Flood generation, Flood
detention, Flood event
Plague control Forest plague frequency – Leaf lignin content + Plague frequency, Disease
Abundance insectivorous Polyphenol content + frequency, Tree
species + pathogens, Natural pest
control, Pest control,
Biological control,
Biological pest control
Pollination Pollinator visitation rate to Pollinat*, Pollination
flowers + service, Pollinator
efficiency, Flower
visitor, Zoophilous
Pollution regulation Soil NOx emissions – Concentration of heavy Air purification, Air
metals in tissues + clean*, Pollut*,
Plant isoprene emissions – Contamination, Noise,
Plant monoterpene BVOC, Biogenic
emissions – emission*, Volatil*,
Plant NOx emissions – Water quality, Water
purification, Water
clean*, Sequestration,
Mining
Soil erosion control Leaf litter production + Litter layer mass/depth + Root depth + Soil erosion, Weathering,
Root mass per unit soil Soil loss, Sediment,
area + Root depth, Root
Understorey biomass + density, Erosion
protection, Soil
stability, Sand stability,
Root depth, Root
density, Soil erodibility,
Soil floor
Table 1. Continued
Target variables
Regulating ecosystem Ecosystem/community Key words used in the
services Ecosystem processes properties Plant species traits literature search†
Soil fertility Canopy nutrient content Leaf nutrient content + N fixation, (Soil, Leaf,
+ Litter nutrient content + Leaves, Litter) AND
Carbon exchange capacity (Nutrient*, Nitrogen,
+ Phosphorus, CEC)
Soil base saturation +
Soil nutrient content +
Soil formation Infiltration rate of Litter layer mass/depth + Hyphal length + LMA, SLA, SLM,
nutrients + Root mass per unit soil Litter C:N – Nitrogen, Phosphorus,
Litter accumulation rate area + Litter lignin – Lignin, Litter
+ Soil invertebrate Litter lignin:N – decomposition, Litter
Litter decomposition rate abundance + C:N, Litter C/N,
+ Soil organic matter + Mineralization,
Mineralization rate + Nitrification,
Nutrient input by litterfall Ammonification, Soil
+ respiration, Microbial
Soil microbial activity + biomass, Soil organic
Soil respiration rate + matter, Soil
compaction, RGR,
Growth rate, Litter
layer, Litter?fall, Soil
invertebrates, Root
specific length, Hyphal
length
Water regulation Canopy interception of Canopy water content + Sap flow rate + Canopy water content,
rainfall + Leaf area index + Stomatal conductance Soil moisture, Runoff,
Evapotranspiration + Litter layer mass/depth + +/– LAI, Litter layer,
Infiltration rate + Soil moisture + Transpiration rate + Evapotranspiration,
Water repellency – Tree water consumption Infiltration, Water
rate + recharge,
Water use efficiency + Transpiration, Sap
flow, Stomatal
conductance, Water use
efficiency
†Compound key words were introduced between inverted commas.
For timber products, we performed an intensive search across species. Moreover, information on productivity per
of country reports where information on provisioning of species at the region/state level was generally not available
harvested timber (m3 y –1 ) was available per species, at for several of these 16 categories. To overcome these
country or sub-country (state or administrative region) level, limitations, we compared the uniqueness in the production of
for the period 2007–2015. The difference between the non-timber products between NNTs and NTs. Uniqueness
proportion of timber provided by NNTs and by NTs was was recorded as the number of categories of non-timber
calculated as the effect size for each country/region (i.e. case products (N = 0–16) that could be obtained only from
study). A positive value indicates a higher timber provision NNTs or only from NTs at country level (e.g. in Spain
by NNTs than by NTs, and vice versa (see Appendix S5 for and Portugal, cork is exclusively produced by a NT, so this
further details). product counts as unique to NTs; by contrast, honey can
For non-timber products, we considered 16 categories, derive from both NTs and NNTs, thus not counting as
following the classification of the Secretariat of the unique to any group). We compiled data for a total of 16
Convention on Biological Diversity (https://www.cbd countries, each one representing a case study.
.int/doc/publications/cbd-ts-06.pdf; Appendix S5). Fruits To assess whether NNTs have higher non-timber
obtained from tree crops were excluded because they come uniqueness than NTs in each country, we calculated the
from non-forest land cover zones. Given that production effect size using the log odds ratio under Peto’s method
of different non-timber products is often species specific (logORP ), which is frequently used in meta-analyses to
and may differ in orders of magnitude across products (e.g. aggregate data reported as frequencies. The logORP is
cork production is expressed in t ha –1 y –1 , while honey and the difference between an observed value and the value
edible fungi in kg ha –1 y –1 ) they could not be aggregated expected by chance in a contingency table (Borenstein
et al., 2009). In this case, the observed value was the (e) Predictors of the variation of NNT effects on ecosystem (dis) services
number of non-timber categories unique to NNTs, while
Based on previous knowledge (Brundu & Richardson, 2016;
the expected value was calculated from the number of
Castro-Díez et al., 2014a; Kull et al., 2011; Vilà & Pujadas,
NNT and NT species present in the country, expecting
2001) we selected a set of nine predictors to explain the
that both groups have the same uniqueness for non-timber
variation of NNT effects on ecosystem (dis)services (Table 3).
production (for further details on logORP calculation see
For RES, we selected one biogeographic predictor (biome),
Appendix S4B). A positive logORP value indicates that NNTs two properties of the vegetation structure (native ecosystem
supply more unique non-timber product categories than type and NNT stand type), one functional property of
expected according to the proportion of NNT species in NNTs (N-fixing), and the phylogenetic relatedness between
the country. Specific sources of information are shown in species (see Section II.2b). Biome was selected because the
Appendix S5. literature suggests that the effects of non-native plants on the
nutrient cycle depend on the large-scale climatic conditions,
(c) Cultural ecosystem services (CES) as captured by biomes (Castro-Díez et al., 2014a). The type
of native ecosystem (e.g. grassland, shrubland, forest, etc., see
CES cover non-material benefits people obtain from ecosys- categories in Table 3) was included to account for the gross
tems through spiritual enrichment, cognitive development, functional distance between the NNT and the dominant
reflection, recreation, and aesthetic experiences (MEA, control vegetation, a key factor to explain the magnitude of
2005). These benefits were grouped under five categories: the impacts caused by non-native plants (Castro-Díez et al.,
recreation and ecotourism, aesthetic, inspiration, cultural 2014a; Chapin et al., 1996; D’Antonio & Corbin, 2003).
heritage and scientific interest (MEA, 2005). For each CES The type of NNT stand (whether planted or naturalized)
category we selected at least one representative source of may explain variations in the effects of NNTs on RES
quantitative information (Vaz et al., 2018). For example, as because of different functioning between an artificial (planted)
sources for aesthetic value, we selected catalogues of orna- stand and a spontaneous self-maintained system (forest with
mental plant dealers and catalogues of species present in naturalized NNTs) (Cruz-Neto et al., 2018; Paz et al., 2015).
urban parks (see Table 2 for all CES sources and Appendix Finally, the N-fixing ability of NNTs was selected because
S6 for further details). For each case study (e.g. each cat- of its well-known effect on soil properties and processes
alogue), we calculated the effect size using the logORP (as (Castro-Díez et al., 2014a; Liao et al., 2008; Vilà et al., 2011).
in Section II.1b). In this case, the observed value was For PES, CES, and EDS we also selected biome, plus two
the frequency of NNT species in the CES source; the indicators of socio-economic development (gross domestic
expected value was calculated assuming that both NNT product and human development index), two demographic
and NT species have the same chances of being included predictors (population density and proportion of rural
in the source (Appendix S4B). LogORp values higher or population), and an index of human disturbance (ecological
lower than 0, respectively, indicate an increase or decrease footprint) (Table 3). Socio-economics and demography are
in the particular CES caused by NNTs. Data on CES recognized determinants of people’s demands for resources
were collected for different regions/states for most coun- and their perception of cultural assets from non-native plants
tries. For USA, only data for Hawaii could be collected. (Kueffer, 2017; Kull et al., 2011; Vaz et al., 2018; Vilà &
In total, our database contained 938 case studies from Pujadas, 2001). The numeric predictors were not significantly
13 countries. correlated in our data set (Spearman’s rank correlation test:
r s < 0.045, P > 0.05). Information on the sources used to
obtain these predictors and the rationale for their selection
(d) Ecosystem disservice (EDS)
is shown in Appendix S7.
The contribution of NNTs to the EDS pollen allergenicity
was assessed using the same procedure described for CES. (2) Data analyses
In this case, the source of information was the Allergome
website (www.allergome.org), which compiles worldwide (a) Computation of grand mean effect size
information on allergenicity of plant species. For each of To assess the contribution of NNTs to the provision of each
62 countries/regions we counted the number of NNT and ecosystem service across RES, PES CES and EDS (with
NT species with and without allergenic pollen, using the lists the exception of timber provision, see below), all effect sizes
of tree species present in each country. We then calculated (Hedges’ d or logORP ) obtained for each ecosystem (dis)
the effect size using logORP , in which the observed value service were combined using a random effects meta-analysis
was the frequency of NNT species producing allergenic model (REMA) to provide a grand mean effect size [either
pollen. The expected value was calculated assuming that d + for numerical data (RES) or logORw for frequency data
both NNTs and NTs have the same chances of being (non-timber PES, CES and EDS)], where the weight of each
allergenic (see Table 2 and Appendix S4B). LogORp values case study was the reciprocal of the case study variance. In a
higher or lower than 0, respectively, indicate a higher or lower random-effects model, the variance of each study results from
contribution from NNT species to the EDS than expected by the variability within (i.e. sampling error) and among case
chance. studies (i.e. the random component). We calculated the latter
8
Table 2. Sources of information associated with different categories of cultural ecosystem services (CES) and one disservice (EDS), pollen allergenicity. Calculation of the log
odds ratio under Peto’s method (logORP ) was based on the difference between the observed non-native tree (NNT) value in a given source (A) and the expected NNT value
under the assumption that both NNTs and native trees (NTs) have the same chances of being included in the source: (A+B)×(A+C)/(A+B+C+D). For further details see
Appendices S4B and S6. Information was collected mostly at the sub-country level (state or administrative region). No., number.
Values observed in the source associated

with a given (dis)service Values used as control
Cultural ecosystem Sources of
(dis)services information Rationale NNT in the source (A) NT in the source (B) NNT in the control (C) NT in the control (D)
Aesthetics Catalogues of Tree species offered by No. of NNT species No. of NT species No. of NNT species No. of NT species
ornamental plant plant dealers are offered in catalogues offered in catalogues present in the country present in the
dealers appreciated mostly for country
their aesthetic values
Tree inventories of Tree species exhibited in No. of NNT species No. of NT species No. of NNT species No. of NT species
urban parks urban parks are included present in inventories present in present in the country present in the
mostly for their aesthetic inventories country
values
Recreation and Official tourism Photographs from tourism No. of photographs No. of photographs NNT cover in the region NT cover in the region
ecotourism websites websites were selected for dominated by NNTs dominated by NTs
the potential of NTs or
NNTs to attract tourists,
constituting motivations
for tourism
Nature routes from Geo-referenced nature No. of route photographs No. of route NNT cover in the region NT cover in the region
Wikiloc routes shared with the dominated by NNTs photographs
public were a mean of dominated by NTs
assessing society
preferences for recreation
and tourism
Cultural heritage Official lists of Monumental trees represent No. of NNTs in the list No. of NTs in the list NNT cover in the region NT cover in the region
monumental symbols of culture and
trees history, relating to
human ‘sense of place’
Inspiration Collective websites Artistic photographs reflect No. of photographs No. of photographs NNT cover in the region NT cover in the region
of artistic nature the choice of inspiring dominated by NNTs dominated by NTs
photographs motifs from nature
Scientific interest Scopus database of The number of scientific No. of publications on No. of publications on No. of NNT species No. of NT species
peer-reviewed publications on NNT or NNTs NTs present in the country present in the
scientific NT species in a country country
literature indicates the scientific
interest on these species
groups in that country
Pollen allergenicity Pollen allergenicity The allergenic potential of a No. of NNT species No. of NT species No. of NNT species not No. of NT species not
from the tree reduces the benefit of producing allergenic producing allergenic producing allergenic producing allergenic
database human–nature pollen pollen pollen pollen
allergome.org interactions
Pilar Castro-Díez and others
Table 3. Predictors used to explain the variation of non-native tree (NNT) effect size on ecosystem (dis)services across case studies.
The last column indicates the category of ecosystem service to which the predictor was applied (RES, regulating; PES, provisioning;
CES, cultural ecosystem services; EDS, ecosystem disservice).
Applied to ecosystem
Acronym Description Predictor categories service category
(Bio)Geographic context
1. Biome Biome of the study site or Tropical forest∗ RES, PES, CES, EDS
dominating in the Subtropical forest
country Subtropical desert
Mediterranean
Temperate forest
Temperate grassland/desert
Boreal forest
Stand and species properties
2. Ecosystem Native ecosystem type (Semi)desert RES
Grassland
shrubland
Open forest
Forest
Urban
3. Stand type NNTs in forest plantations NNTs in planted stands RES
or naturalized NNTs in naturalized stands
4. N-fixation NNT is N-fixing or not NNTs N-fixing RES
NNTs not N-fixing
Socio-economic development
5. GDP Nominal gross domestic Numeric data CES, PES, EDS
product (US Dollars)
6. HDI Human Development Numeric data CES, PES, EDS
Index (ranking values)
Demography
7. PopDens Population density (km-2 ) Numeric data CES, PES, EDS
8. RurPop Proportion of rural Numeric data CES, PES, EDS
population (%)
Human disturbance
9. EFP Ecological footprint Numeric data CES, PES, EDS
(ranking values)
∗
The term ‘forest’ is used here in a broad sense, including also savannahs and woodlands.
using the restricted maximum-likelihood estimation (REML) (publication, NNT species or country) as random factor
for numeric data, and the DerSimonian-Laird (DL) model for (Nakagawa & Santos, 2012). These models allow for different
frequency data (Borenstein et al., 2009; Viechtbauer, 2010), variations of effect sizes between case studies within the same
using the rma() function implemented in the R package level of the random factor. MLMA models were fitted using
metafor (Viechtbauer, 2010). This function also provides the rma.mv() function in metafor. Differences in fit between the
the 95% confidence intervals for each grand mean effect REMA and MLMA models were assessed using the Akaike
size and a two-tailed parametric test checking whether Information Criterion corrected for small sizes (AIC c ), so that
the effect size differs from zero. Given the non-normal the more complex models (MLMAs) are considered to be
distribution of the residuals of some models, we additionally an improvement on the simplest one (REMA) if they result
assessed the two-tailed significance of each grand mean effect in a reduction of AIC c of two points or more (Burnham &
size through non-parametric permutation tests under 1000 Anderson, 2004; Senior et al., 2016).
iterations using the permutest() function from package metafor In the case of timber provision, the effect size of each case
(Viechtbauer, 2010). study was the difference between the proportions of timber
In our data sets some case studies were derived from the provided by NNTs and by NTs, with no associated variance.
same publication (RES), or refer to the same NNT species Case studies were in most cases the largest administrative
(RES), or come from the same country (RES, PES and CES), regions below the country level (equivalent to European
and thus may be more closely related to each other than to NUTS-2), but for six countries (Bulgaria, Czech Republic,
other case studies. To explore if non-independence affected Chile, Ireland, New Zealand, and Portugal) data were only
the results, we additionally assessed the grand mean effect size available at the country level. The grand mean effect size
and its significance using multi-level meta-analysis models (±95% confidence intervals) was calculated as the weighted
(MLMAs), each including one source of non-independence median (due to non-normal distribution) across all case
studies. The weighting factor was the proportion of all global of evolution, and approach 0 when there is no phylogenetic
timber produced by each country/region (multiplied by signal.
1000 for scaling reasons), so that country/regions with larger To explain the variation of NNT effects on timber
annual timber harvest (NNT+NT) contributed more to the provision, separate linear models were conducted with the
grand mean effect size. A two-tailed Wilcoxon rank test was R function lm() to assess the effects of the biome and
computed to assess whether the grand mean effect differed socio-economic predictors in Table 3. In some cases, effect
from zero, using the wilcox.test() function in R. sizes were aggregated at the country level before performing
the linear models to match the scale at which predictors were
available. Country was tested as an additional predictor,
(b) Computation of heterogeneity and structured meta-analyses as this data set did not allow us to perform a MLMA
For each grand mean effect size calculated with REMA with country as a random factor (see Section II.2a). In the
(either d + or logORw ), we computed the heterogeneity across analysis of country, the six countries where timber provision
effect sizes using several statistics: (i) the Q T statistic is the sum was only available at country level were removed from
of squares of the deviations of each effect size from the grand the analyses. To improve homoscedasticity, the effect size
effect size, weighed by the inverse of the effect sizes’ variances. (the difference between the proportions of timber provided
Q T was tested against a chi-squared distribution with n–1 by NNTs and by NTs) was transformed according to the
degrees of freedom (n = number of case studies) to assess formula: arcsine (sign(x) × sqrt(abs(x))). To compensate for
whether the observed heterogeneity is greater than expected the different contribution of each case study to global timber
by chance (Borenstein et al., 2009). The caveat of the Q T production, the weighting factor was included in all linear
statistic is that its reliability and significance depend on the models with the R function offset().
number of case studies (Borenstein et al., 2009; Nakagawa &
Santos, 2012). Thus, we computed two additional statistics; (c) Publication bias
(ii) T 2 which is the estimate of the between-case study Meta-analysis results may be affected by publication bias,
variance; and (iii) I 2 which is the proportion (in %) of the i.e. the selective publication of articles finding significant
total variation in effect sizes that is due to the between-study effects over those which find non-significant effects (Begg,
variance (T 2 ) (Borenstein et al., 2009; Nakagawa et al., 2017). 1994). Publication bias for each RES was investigated by
The three statistics were calculated using the rma() function exploring asymmetry in a funnel plot, with effect sizes on
of the metafor R package. In the case of the MLMA models, the x-axis and standard error of effect sizes on the y-axis. In
we partitioned I 2 between the random factor level and the the absence of publication bias, this plot is expected to be
case study level following Nakagawa & Santos (2012). a symmetric funnel shape, with a larger dispersion of effect
We further assessed whether the variation of effect sizes for studies with smaller sample size, i.e. those with large
sizes could be explained by the predictors (fixed factors) standard errors of effect size (Borenstein et al., 2009). We
shown in Table 3. We performed random-effects (REMA) assessed funnel asymmetry using the random/mixed-effects
structured meta-analyses using the rma() function, which version of the Egger’s test, which performs a structured
allows incorporating predictors and returns coefficients and meta-analysis with the standard error as predictor, and
an omnibus test assessing whether the coefficient differs returns its slope and significance (Sterne & Egger, 2005).
from zero. For continuous predictors, the function also This test was implemented using the regtest() function
provides the regression slope and its significance. Given of the metafor package (Viechtbauer, 2010). A significant
the non-normal distribution of residuals in many cases, relationship implies asymmetry in the funnel plot, which
we additionally assessed the two-tailed significance of the may be an indication of publication bias due to missing
predictors over 1000 iterations with the permutest() function values on one side of the funnel. However, there are other
(Viechtbauer, 2010). reasons for funnel asymmetry besides publication bias, such
In the case of RES, we also tested for a phylogenetic signal as heterogeneity (Nakagawa & Santos, 2012; Viechtbauer,
on the NNT effects using the Phytools R package (Revell, 2010). Thus, when the Egger’s test on the meta-analysis
2012). We first constructed a phylogeny of NNT species, without predictors indicated asymmetry, we repeated the
starting from the time-calibrated molecular phylogeny of test on the meta-analysis with the predictor which explained
Zanne et al. (2014). We selected the taxa of our study more heterogeneity. If this test still reported asymmetry, we
(at genus level) using the congeneric.merge() function; then assessed the impact of publication bias by removing case
we pruned the phylogeny with the drop.tip() function to studies responsible for funnel asymmetry (Borenstein et al.,
obtain a separated NNT phylogeny for each RES with a 2009), and by applying the trim-and-fill method (Duval &
minimum of 10 species (otherwise the statistical power was Tweedie, 2000). This method uses an iterative procedure to
considered too low). The phylogenetic signal was assessed remove the most extreme small studies from the asymmetric
using two common comparative metrics (Blomberg’s K and side of the funnel plot, then adds the original studies back
Pagel’s λ) (Blomberg, Garland & Ives, 2003; Pagel, 1999). into the analysis, imputes a mirror image for each one, and
Although the rationale behind these metrics is different, re-computes the meta-analysis. If the new grand mean effect
both approach 1 when the species phylogenetic signal size retains the same sign and significance, then we conclude
approximates predictions under a Brownian motion model that publication bias has a trivial or modest impact, but
if there is a shift of the sign or significance of the grand Pinus radiata D. Don, Robinia pseudoacacia L., and Falcataria
mean effect size, then the impact of publication bias may be moluccana (Miq.) Barneby & J.W. Grimes) were the best
substantial (Nakagawa & Santos, 2012). represented, with 20–22 case studies; four additional species
(Acacia saligna (Labill.) Wendl., A. longifolia (Andrews) Willd.,
(d) Synergies and trade-offs between ecosystem (dis)services Eucalyptus globulus Labill., and Ligustrum lucidum W.T. Aiton)
were represented by 10–17 case studies. At the other
Some variables are simultaneously involved in multiple extreme, 44 NNT species were each represented by a single
services, which may lead to synergies and trade-offs among case study (Table S1). The PES, CES and EDS data sets
services within and among categories (Cord et al., 2017; de covered the (dis)services provided by all NNT versus all NT
Groot, Wilson & Boumans, 2002). For instance, depth of species of a country or region (see Section II.1); thus, the list
the litter layer is positively related to soil formation but of NNT species was not specified in this case.
negatively to fire-risk prevention (see Table 1), which may
lead to trade-offs between these services. We checked for
(2) Effects of non-native tree species on regulating
the existence of positive and negative relationships among
ecosystem services
the effects of NNTs on different ecosystem (dis)services.
Given that the unit of observation differed across types of Our random-effects meta-analysis (REMA) of 529 case
ecosystem (dis)services (NNT species for RES versus country studies obtained from the scientific literature revealed
or administrative region for PES, CES and EDS), associations that NNTs increased climate regulation, soil fertility, soil
were evaluated through two separate analyses. For RES, we formation and soil erosion control, but decreased fire-risk
computed the mean effect size (d + ) of each NNT species on prevention (Fig. 2A). Asymmetry in funnel plots (Fig. S3)
each service and tested for significant correlations among the and Egger’s tests suggest the presence of publication bias
effects of the same NNT species on different RES. For PES, for climate regulation, soil fertility and fire-risk prevention;
CES and EDS, we calculated the mean effect size (logORw ) for however, the asymmetry of the latter disappeared when
each country/region, and analysed the correlations among ecosystem type was included as predictor (Table S2).
the NNT effects found in the same countries/regions on For climate regulation and soil fertility, the trim-and-fill
different PES, CES and EDS. We used pairwise Spearman procedure did not change the mean effect size, suggesting
rank correlation tests in R software. that the impact of publication bias was trivial (Table S2). In
R codes and part of the data used in this study are available addition, the removal of the six case studies responsible for
in the repository Consorcio Madroño (doi: 10.21950/EGM8SE). the funnel asymmetry in the soil fertility data set (see Fig.
S3) resulted in a smaller, but still significant, mean effect
size (d + shifted from 0.63, P = 0.012 to 0.46, P = 0.027).
III. RESULTS For pollution regulation, pollination and water regulation we
found no significant effects of NNTs (Fig. 2A).
Compared with REMA, MLMA including either refer-
(1) Description of the data set
ence, country or NNT species as a random factor, generally
We analysed a total of 1683 case studies (529 on RES, 154 improved the model’s explanatory power (AIC c reduction
on PES, 938 on CES, and 62 on the EDS pollen allergenicity). ≥2). However, results were largely consistent between
Data covered 44 countries (33 on RES, 22 on PES, 13 on CES REMA and the MLMA. The only exceptions were soil fertil-
and 13 on EDS), all continents except Antarctica, and seven ity and soil formation, which were not significantly affected
biomes (Fig. 1). Continents with developed countries, such by NNTs when NNT species (soil fertility) or country (both
as Europe, were over-represented with respect to their size, RES) were added as random factor in MLMA (Table S3).
whereas large continents such as Asia and Africa were The heterogeneity of NNT effects across case studies was
under-represented (Fig. S1). Temperate, mediterranean and high (I 2 > 80%) for all RES except pollination, Fig. 2A,
tropical biomes accounted for most case studies, while other Table S3). Biome explained the heterogeneity of effects on
biomes were less (boreal forest, subtropical forest and desert, climate regulation, soil formation and soil erosion control
and temperate grassland/desert) or not (polar) represented (Table S4), with larger effects in low-latitude biomes (tropical
(Fig. S2). and subtropical forests) than in middle-latitude biomes
The best represented ecosystem services were soil (mediterranean and temperate forest) (Fig. 3A–C). Fire-risk
formation (RES), soil fertility (RES), timber provision prevention was more decreased by NNTs in shrublands
(PES), recreation and ecotourism (CES), and aesthetics than in grasslands and forests (Fig. 3D). The increase of
(CES), with more than 115 case studies each. The least soil fertility and formation by NNTs was greater in stands
represented ecosystem services were pollution regulation of naturalized NNTs than in NNT plantations (Fig. 3E,
(RES), pollination (RES), non-timber provision (PES) and F). Finally, higher increases of soil fertility, soil formation,
scientific interest (CES), with less than 20 case studies each soil erosion control, and water regulation were found when
(Fig. 2). For plague control and flood regulation (RES), no NNTs were N-fixing (Fig. 3G–J). The remaining effects of
valid case studies were found. predictors on RES were non-significant (Table S4). The
Our RES data set covered a total of 125 NNT species. ability of the Fabaceae clade (encompassing N-fixing species)
Among them, four species (Ailanthus altissima (Mill.) Swingle, to contribute most to soil fertility and soil formation was
Fig. 1. Simplified representation of the distribution of case studies. Data were collected to evaluate worldwide effects of non-native
tree species on regulating (RES), provisioning (PES) and cultural (CES) ecosystem services and ecosystem disservices (EDS). For
simplicity only RES are represented at the local scale (dots), whereas data for PES, CES and EDS are represented at the country
scale (flags). The map shows the biomes considered in this study for illustrative purposes (simplified from the FAO Global Ecological
Zones). The term ‘forest’ is used in a broad sense, including also savannahs and woodlands.
also reflected in the significant values of Pagel’s λ, which On the basis of the information collected for 16 countries,
indicated a phylogenetic signal in these effects. However, for we found less uniqueness of non-timber products in NNTs
the rest of RES, neither Pagel’s λ nor Blomberg’s K show than NTs, i.e. there are more categories of non-timber
a phylogenetic signal attributable to a Brownian model of products that are exclusively obtained from NTs than from
evolution (Table 4). NNTs (Fig. 2B).
(3) Effects of non-native tree species (4) Effects of non-native tree species on cultural
on provisioning ecosystem services ecosystem services
From our global data set of 144 case studies obtained from Our global data set revealed that NNTs have a wide
worldwide forestry reports, we found that the proportion range of effects on the five CES categories considered.
of timber obtained from NTs was slightly higher than According to REMA results, NNTs increased aesthetic values
that obtained from NNTs (Fig. 2B). ANOVA tests showed determined from catalogues of plant dealers and inventories
large differences in NNT effects across biomes (F = 6.07, of urban parks. For recreation and ecotourism, NNTs
P < 0.001), and across countries (F = 17.91, P < 0.001). were present more often in ecotourism websites, but less
Timber production in the subtropical forest biome relied in nature routes than NTs than expected by chance
mostly on NNTs while temperate and boreal biomes relied (Fig. 2C). NNTs increased cultural heritage (i.e. they were
more on NTs (Fig. 4A). Some countries obtained timber over-represented in catalogues of monumental trees) but
mostly from NNTs (Argentina, Chile, Ireland, New Zealand, have less scientific interest (i.e. they are the subject of fewer
South Africa, UK), while others relied almost exclusively on scientific publications, according to the Scopus database) than
NT (Austria, Bulgaria, Canada, Czech Republic, Germany, NTs (Fig. 2C). We found no effects of NNTs on inspiration
Japan, Switzerland, USA – with the exception of Hawaii) (assessed from the frequency of occurrence in artistic
(Fig. 4B). photographs) (Fig. 2C). Including country as a random
Among the five uncorrelated socio-economic and factor in MLMA improved all models (i.e. explained a high
demographic predictors, only the proportion of rural proportion of the residual between-case studies variance (I 2 )
population was negatively related to the effect size and decreased the AIC c by at least two units, Table S6), but
(slope = –0.04, P = 0.002), indicating that regions with a results were consistent with those of REMA for most CES.
higher proportion of rural population rely less on NNTs for The only exception was recreation and ecotourism, where
timber provision (Table S5). the negative selection of NNTs for nature routes was not
Fig. 2. Effects of non-native tree (NNT) species on ecosystem services assessed using the random-effects model (REMA). The mean
effect size of NNTs and 95% confidence intervals are depicted across the set of case studies considered for each regulating (A),
provisioning (B) and cultural (C) ecosystem services (sample sizes are indicated next to each service). Positive or negative mean effect
sizes, respectively, indicate that NNTs (or sites dominated by NNTs) had greater or smaller scores for the service, compared to
native tree (NT) species or to control sites dominated by native vegetation. Asterisks to the right of the bars indicate that the mean
effect size differs significantly from zero according to a permutation test with 1000 iterations. Values on the right axis indicate the
heterogeneity I 2 , which is the proportion (in %) of the total variation in effect sizes that is due to between-study variance.
significant when country was included as random factor in recreation and ecotourism (Table S7). NNTs contributed
MLMA (Table S6). more to aesthetics in tropical and temperate biomes than
Heterogeneity of effect sizes across case studies was high in mediterranean and boreal ones, and NNTs were used
for most CES (I 2 > 80%, except for recreation/ecotourism more in tourism websites in the mediterranean than in other
and inspiration, Fig. 2C, Table S6). Biome contributed to biomes (Table S8). In countries with higher gross domestic
explaining the variation of NNT effects on aesthetics and products, NNTs contributed more to aesthetics, and were
Fig. 3. Predictors explaining the effects of non-native tree (NNT) species on regulating ecosystem services (RES) under random-effects
structured meta-analysis: biome (A–C), native ecosystem type (D), stand type (E, F) and N-fixation of the NNT (G–J). The figure
shows the mean effect size (d + ) of NNTs and 95% confidence intervals across the set of case studies considered for each predictor
category. Positive or negative mean effect sizes, respectively, indicate that sites dominated by NNTs had a greater or smaller score
of the RES than control sites with native vegetation.
Table 4. Results from two common metrics used in comparative analyses (Blomberg’s K and Pagel’s λ) to test for a significant
phylogenetic signal in the effects of non-native trees (NNTs) on regulating ecosystem services (RES). Each cell contains the value of
the metric and its significance (P) according to the expectation of a Brownian model of evolution. N represents the number of NNT
species in each RES. Significant results (P < 0.05) are indicated with asterisks.
Climate Fire-risk Pollution Soil Soil Soil Water

Metric regulation prevention regulation erosion control fertility formation regulation
Blomberg’s K (P) 0.025 (0.859) 0.184 (0.289) 0.456 (0.588) 0.056 (0.686) 0.543 (0.091) 0.063 (0.687) 0.087 (0.661)
Pagel’s λ (P) 0.000 (1.000) 0.001 (1.000) 0.001 (1.000) 0.117 (0.326) 1.006** (0.001) 0.393* (0.037) 0.001 (1.000)
N 54 35 14 37 56 79 57
more used in tourism websites, but they were selected less population, NNTs contributed less to aesthetics but more
often for nature routes. In countries with higher values of to recreation and ecotourism. The contribution of NNTs
the human development index, NNTs had less effect on to cultural heritage declined at higher population density.
aesthetics and recreation and ecotourism services, suggesting NNTs were less selected as recreation and ecotourism, and
larger effects in less-developed countries. In countries with inspiration assets in countries with larger ecological footprints
higher population density or with a higher proportion of rural (i.e. human disturbance, Table S7).
Fig. 4. Effect size of non-native trees (NNTs) on timber provision across biomes (A) and across countries (B). For each biome/country
the horizontal band represents the median; box limits are defined by the 25th and 75th percentiles; upper whiskers are the smallest
of the maximum country/biome value and 75th percentile + 1.5 × box extension; lower whiskers are the largest of the smallest
biome/country value and 25th percentile – 1.5 × box extension. Circles indicate extreme values outside the whisker interval. The
number of case studies in each biome/country is indicated (biomes/countries with less than three case studies were not included in
the statistical analysis).
(5) Effects of non-native tree species on the products. Finally, pollen allergenicity was increased less
ecosystem disservice by NNTs in countries with a higher proportion of rural
population (Table S7).
Overall, NNTs producing allergenic pollen were not more
frequent than expected, either using REMA or MLMA with
country as a random factor (logORw ± SE = 0.093 ± 0.197
and 0.587 ± 0.365, with REMA and MLMA, respectively, (6) Relationships between ecosystem services
P > 0.05, N = 62, Table S6). Nevertheless, NNT effects on The effects of NNTs on several RES were correlated
pollen allergenicity varied widely with context (I 2 = 91%). with each other. Most Spearman correlations were positive
In tropical and temperate biomes, NNTs contributed more [i.e. among soil fertility, soil formation and erosion
to pollen allergenicity than in mediterranean and boreal ones control, as well as climate regulation, and water regulation
(Table S8). Higher NNT contribution to pollen allergenicity (RS = 0.41–0.68, P = 0.010–<0.001)]. However, fire-risk
was also associated with countries with higher gross domestic prevention was negatively correlated with other RES
(RS = –0.69 and –0.67, P < 0.001 for soil erosion control a trait often selected for NNT introduction (Richardson,
and water regulation, respectively, Table S9). 1998; Woziwoda, Kopec & Witkowski, 2014). Increased
The overall effects of NNTs on PES, CES and productivity of forests may promote climate regulation (via
EDS within countries/regions were somewhat correlated. carbon uptake), and soil formation, fertility and erosion
The most significant was a positive correlation between control (through higher root growth and/or the supply
the two sources of information used for aesthetics, i.e. of more organic matter to the soil) (Evans, 2009; Mori,
catalogues of plant dealers and urban parks (RS = 0.89, Lertzman & Gustafsson, 2017). The decrease in both timber
P > 0.001). Aesthetics was also positively correlated with and non-timber PES by NNT was unexpected, given that
pollen allergenicity (RS = 0.56–0.65, P = 0.01), suggesting the purpose of many tree introductions is the supply of
that many ornamental NNTs produce allergenic pollen. particular products (Brundu & Richardson, 2016; Evans,
Uniqueness of non-timber products was negatively related 2009; MacDicken, 2015). In the case of timber, this is
to pollen allergenicity (RS = –0.71, P = 0.03). Although because many temperate regions rely almost exclusively on
marginally significant, countries where the contribution of NTs. The lower uniqueness of non-timber products found for
NNTs to pollen allergenicity was higher tended to show NNTs suggests that many of these species were introduced to
higher scientific interest in NNTs (RS = 0.58, P = 0.06, increase the quality or quantity of products already supplied
Table S10). by NTs, rather than to produce novel products (Krumm &
Vítková, 2016). Regarding CES, the ornamental value of
non-native plants was previously reported to be associated
with the human preference for novelty and unusual features,
IV. DISCUSSION e.g. the colourful or large flowers of Jacaranda and Magnolia,
the crown shape and size of Sequoia and Ficus (Kueffer &
(1) The data set Kull, 2017; van Wilgen & Richardson, 2012). This may
Our study is the first comprehensive global analysis of the explain the selection of NNTs as aesthetic, tourist and
effects of NNTs on ecosystem (dis)services that brings heritage assets (Vaz et al., 2018). However, this does not
together information from a broad spectrum of scientific explain the reduced touristic value of nature routes caused by
subjects, as well as from online sources. Despite the global NNTs. Ornamental NNTs are usually confined to gardens or
scope, information was more abundant for developed urban parks. Outside these areas, NNTs can occur because
countries, mediterranean and temperate forest biomes, they were planted for non-aesthetic purposes (e.g. timber
and for tree species with high societal interest. This production or land reclamation), or as naturalized escapes
geographical and taxonomic bias is well documented in the from plantations. The traits that promote non-aesthetic uses
ecological literature (Hulme et al., 2013; Martin, Blossey & of NNTs (e.g. fast growth; Richardson, 1998), or those
Ellis, 2012; Pyšek et al., 2008; Wilson et al., 2007). Human associated with naturalization success (e.g. profuse seed
population and forest cover are unevenly distributed across production or resprouting capacity; Castro-Díez et al., 2011;
biomes, and scientific institutions are more abundant in Richardson & Rejmánek, 2004) can lead to monotonous
wealthy regions (Wilson et al., 2007). Our RES data set and homogenized landscapes which are apparently less
covered one third of the 430 NNT species known to be attractive to users of nature routes. Despite the growing
invasive (Rejmánek & Richardson, 2013), of which just number of studies on non-native species (Hulme et al., 2013),
22 species accounted for half of the case studies. This fact the scientific interest in NNTs was overwhelmingly lower
highlights that scientists repeatedly target the few species with than for NTs. This may be because ecological interest in
known large impacts on social-ecological systems (Hulme non-native species and their impacts is recent compared to
et al., 2013; Pyšek et al., 2008). The coverage of ecosystem the long history of research on pristine habitats and native
services was limited by the need to find measures suitable species (Hulme et al., 2013; Vaz et al., 2017a).
for pairwise comparisons and by the need to harmonize data Given that biodiversity often promotes multiple ecosystem
across multiple countries. Despite these limitations, this study services in forests (Gamfeldt et al., 2013; Mori et al., 2017;
offers the most complete and up-to-date analysis of current Poorter et al., 2015), the increase of ecosystem services by
knowledge on NNTs worldwide, and allowed us to identify NNTs found here seems at odds with the low biodiversity
key gaps for future research. usually found in NNT-dominated systems (Gaertner et al.,
2011; Pyšek et al., 2012; Vilà et al., 2011). Our results may
have been exacerbated by the fact that the baseline for
(2) Effects of non-native trees on ecosystem services
comparison may include degraded or non-forest ecosystems.
Overall, we found more increases than decreases in Moreover, replacing NTs with NNTs may maximize a
ecosystem services attributable to NNTs. This result is particular ecosystem service at the expense of reducing the
consistent with many NNTs having been deliberately ecosystem’s capacity to provide multiple services (Dickie
introduced to create or enhance particular ecosystem services et al., 2014a; Evans, 2009; van Wilgen & Richardson,
(Brundu & Richardson, 2016; Evans, 2009; Potgieter et al., 2012), and most studies covered herein focus on single,
2017). The increase in several RES due to the presence rather than multiple, ecosystem services. We also note that
of NNTs may be attributed to their high productivity, maximizing some particular ecosystem services may not
always be beneficial for society or ecosystem functioning. pool of NT species (e.g. because of prevailing slow growth
For example, in the naturally infertile soils of some parts rates, as occurs in the Mediterranean Basin) may have
of Hawaii and the South African fynbos, the increase of favoured plantations of profitable NNTs. Third, some former
soil nitrogen driven by the introduction of N-fixing NNTs European colonies (e.g. Argentina, Australia, Chile, New
is disrupting ecosystem functioning and altering several Zealand or South Africa) have a stronger tendency to plant
ecosystem services, such as soil fertility and water supply NNTs, due to the colonial ethos of ‘national development’,
(Gaertner et al., 2011; Le Maitre et al., 1996; Vitousek & to cultural links with the colonists’ home countries or with
Walker, 1989). Thus, focussing environmental policies on other colonies, or to the loss of native cultures that were more
ecosystem services may overlook the intrinsic value of nature dependent on native species (Carruthers et al., 2011; Speziale
and leave biodiversity under-protected (Dee et al., 2017; et al., 2012). Thus, a complex interaction of environmental,
McCauley, 2006; Silvertown, 2015). social and historical factors seems to have shaped species
selection for PES (Kueffer, 2017). This also explains the
(3) Variability of non-native tree effects poor role of socio-economic and demographic predictors
on ecosystem services worldwide when considered alone. Nonetheless, regions with a small
NNT effects in most ecosystem (dis)services showed medium proportion of rural population (or more urbanised regions)
to high heterogeneity, with I 2 values above 80% in most seem to rely more on NNTs for timber. This suggests that
cases. This high heterogeneity is typical of ecological studies, rural societies tend to rely more on native assets, because
where effect sizes derive from different species and different the populace has a closer connection with the environment
contexts (Senior et al., 2016). Nevertheless, we were able to or less need of resources (Carruthers et al., 2011; Shackleton
explain part of this heterogeneity. Nitrogen-fixing NNTs et al., 2007; Speziale et al., 2012).
had especially strong effects on soil fertility, in agreement Our results showed that NNTs contributed more to
with previous studies (Castro-Díez et al., 2014a; Liao et al., CES in countries with greater nominal gross domestic
2008; Vilà et al., 2011). Compared with non-N-fixing NNTs, products. Wealthy regions foster the trade and maintenance
N-fixing NNTs may attain a higher production in infertile or of non-native plants (Gavier-Pizarro et al., 2010; Humair
degraded soils, explaining their contribution to soil formation et al., 2015; Vilà & Pujadas, 2001), and thus their contribution
(by supplying more organic matter to the soil), and to erosion to CES (Vaz et al., 2018). Nevertheless, NNT contribution
control and water regulation (by a denser protective cover of to aesthetics, and to recreation and ecotourism decreased in
the soil and a greater net of roots belowground). Accordingly, regions with higher human development index (i.e. higher life
the low proportion of N-fixing NNTs among planted expectancy, education level, and income), a trend previously
stands (9.1–14.1%), compared with naturalized stands observed in the Iberian Peninsula (Vaz et al., 2018). This
(41.5–51.2%), may explain the larger effect size of NNTs suggests a higher awareness of the risks associated with
on soil fertility and formation found in naturalized stands. NNTs, and thus a higher preference for NTs as ornamental
Certain RES were more affected by NNTs in low-latitude and tourism assets in more developed regions (Nuñez &
biomes than in temperate biomes, possibly related to the Pauchard, 2010; Vaz et al., 2018). Finally, we found a lower
stronger effect of non-native plants on the nitrogen cycle contribution of NNTs to tourism and inspiration services
in benign climates reported previously (Castro-Díez et al., in regions with larger ecological footprint, suggesting that
2014a). Many NNTs are selected primarily for their high a higher pressure on natural resources makes people prefer
potential productivity (Richardson, 1998; Woziwoda et al.,
NTs as inspirational and tourism assets.
2014), a trait that underpins many ecosystem services.
Some predictors that explain the heterogeneity of NNT
However, that high potential productivity would be realized
effects relate to intrinsic properties of individual NNTs
more in environments where the favourable period for plant
(e.g. N-fixation ability) or to the environments in which
growth is longer (e.g. tropical forests) (Castro-Díez et al.,
2014a). they occur (e.g. biome). Other predictors relate more to
The degree of phylogenetic relatedness among species the social dimension, such as socio-economy, demography,
showed a small role in explaining variation of NNT effects and cultural background. Whereas ecological conditions
on RES. This means that closely and distantly related are expected to be more or less stable in the long term,
species have similar effects. The only phylogenetic signal the social dimension (e.g. human perceptions, norms and
was found for the effects of NNTs on soil fertility and soil values, social memory, institutions and rules) is more prone
formation, and is associated with the phylogenetic proximity to changes in a few generations. This has important
among N-fixing NNTs, which had greater effects on consequences for the way in which NNTs affect ecosystem
these RES. services through time (Kueffer & Kull, 2017; Kull et al.,
The great cross-country and cross-biome variation 2018; Shackleton et al., 2016). There are many examples of
observed in the contribution of NNTs to timber provision people embracing introduced species in their practices and
might be explained by several non-exclusive arguments. First, traditions in preference to native species used previously
regions with high availability or variety of NT species (e.g. (i.e. the ‘shifting baseline syndrome’; Kueffer & Kull, 2017;
USA, Brazil) have less need to introduce NNTs to supply Nuñez & Simberloff, 2005; Speziale et al., 2012). This poses
their timber needs. Second, regions with a non-profitable an additional risk to focusing environmental policies solely on
ecosystem services, whose values for people are changeable (5) Methodological limitations and future
over short time frames (Silvertown, 2015). perspectives
Despite the patterns of variation in NNT effects on
Publication bias in the scientific literature may have affected
ecosystem services revealed here, a large proportion of
our RES analysis. Funnel plot asymmetry suggests that
variation remains unexplained. This suggests that other
the positive effects of NNTs on climate regulation and soil
predictors that were not considered in our analysis are
fertility may have been inflated by publication bias. However,
important, such as NNT functional traits (e.g. plant size,
the two methods applied (trim and fill and removal of case
seed mass or leaf habit; Castro-Díez et al., 2014a; Pyšek
studies from the extreme of the funnel) suggest consistent
et al., 2012), or the historical factors accounting for the
results. Future updates might minimize publication bias,
cultural and trade relations between distant regions through
e.g. by extending the literature search to grey literature
time (Speziale et al., 2012). Other potential predictors may
(Borenstein et al., 2009).
operate at local scales, and thus could not be included in our
Another methodological issue in meta-analysis is
global-scale analysis (e.g. silvicultural practices, individual
non-independence among case studies (Nakagawa &
choices, attitudes, and behaviours; Grove et al., 2006; Kull
Santos, 2012; Noble et al., 2017). Although partly removed
et al., 2018).
by aggregating related case studies, non-independence
remained in our data sets due to multiple case studies
(4) Synergies and trade-offs among the effects derived from the same publication, the same NNT species,
of non-native trees on ecosystem services or the same country. The impact of non-independence on
The correlations found among most RES can be explained results may be assessed by comparing the results from the two
by the fact that some tree traits simultaneously contribute meta-analysis models, MLMA and REMA (with and without
to different RES. In particular, the potential growth rate the source of non-independence as a random factor). Only
of trees may underpin many of the identified links across three ecosystem services (soil fertility, soil formation and
the effects of NNTs on RES: fast-growing trees can be touristic value of nature routes) changed from being affected
important carbon sinks and thus contribute to climate by NNTs (REMA) to a non-significant effect (MLMA with
regulation, while simultaneously promoting erosion control country as random factor, and also with NNT species in
and soil formation through rapid development of a protective the case of soil fertility). This indicates that results for these
soil cover, enhancing soil organic matter, and contributing services cannot be extended to any random set of case
to regulation of the water cycle. Yet, trade-offs across RES studies. For instance, the increase in soil fertility by NNTs
may also arise when the same trait contributes positively was due to N-fixing trees; thus, a data set with fewer N-fixing
to some services and negatively to others (Potgieter et al., NNTs would be likely to return a non-significant result. Also,
2017). Thus, some fast-growing trees can also increase fire the effect of NNTs on the touristic value of nature routes
risk by supplying a high quantity of fuel to the system, varied across countries (e.g. it was decreased in Australia and
and because they invest less resources in protection against Spain, but increased in Italy and South Africa). Thus, the
disturbances (Herms & Mattson, 1992). Regarding CES, we overall decrease may be attributed to the high proportion of
identified a strong correlation between the two sources of case studies from Australia and Spain (Appendix S6). Future
aesthetic information (i.e. catalogues of ornamental plant studies should account for this bias by representing each
dealers and tree inventories of urban parks) indicating strong country with a number of case studies proportional to its
consistency between them. By contrast, the lack of correlation population or size.
between the two indicators of recreation and ecotourism In the case of case of CES, EDS and non-timber PES, we
(i.e. official tourism websites and nature routes) indicates used a novel indicator-based approach, previously described
that they capture different aspects of ecotourism attraction: in Vaz et al. (2018). This approach allows assessing whether
tourism websites may tend to highlight the ‘unusual’ or the NNTs are preferred or rejected for particular services,
‘spectacular’ to attract visitors (e.g. a plantation of sequoias using the ‘offer’ (i.e. availability) of NNTs in the region
in northern Spain or conifers along the Garden Route as a reference value. This approach has the advantage
in South Africa), whereas users of nature routes appreciate of integrating multiple sources of information, allowing
more ‘pristine’ nature dominated by native species (Vaz et al., reproducibility and updates as the sources expand (Vaz
2018). We also found a synergy between aesthetics and pollen et al., 2018). In addition, sources of information from social
allergenicity, suggesting that NNTs with aesthetic value may media (e.g. tourism, image-sharing, or commercial websites)
also exhibit traits that promote pollen allergenicity (e.g. wind have a much wider coverage than traditional scientific
pollination, which was found to increase with urbanization; media (Richards & Friess, 2015; Wood et al., 2013). Yet, the
Williams, Hahs & Vesk, 2015). This result converges with approach has some caveats: lower data quality (e.g. potential
others showing high allergenicity in non-native air-borne mistakes in species names in catalogues); low resolution of
pollen from ornamental NNTs (Belmonte & Vilà, 2004; the analysis (effect sizes are calculated for a group of NNTs
Bosch-Cano et al., 2011). Unfortunately, differences in scale of a country/region, rather than for particular species);
of study used for RES compared with PES, CES and EDS sensitivity of the effect size metric (logORP ) to the choice
precluded us from exploring other synergies and trade-offs of data types and control data (Vaz et al., 2018); or the
across different categories of ecosystem services. inability to compare magnitudes of logORw across ecosystem
(dis)services with data sources provided in different units (e.g. Technology) (www.cost.eu). The work was also supported
species counts, species cover, or number of photographs). In by the IMPLANTIN project (CGL2015-65346-R) of the
summary, this novel approach is useful to obtain preliminary Ministerio de Economía y Competitividad of Spain, and the
insights on the directions of effects of NNTs on certain REMEDINAL3-CM MAE-2719 network (Comunidad de
ecosystem (dis)services assessed poorly by scientific media, Madrid). A.S.V. was supported by the FSE/MEC and FCT
and to cover spatial and temporal scales not attainable (PhD grant PD/BD/ 52600/2014); J.R.V. by POPH/FSE
through traditional scientific methodologies. Future studies and FCT (Post-Doc grant SFRH/ PD/84044/2012); O.G.
should validate our results for specific contexts using other by EU H2020 research and innovation program (Marie
methodologies (Hernandez-Morcillo et al., 2013). Sklodowska-Curie grant agreement No 661118-BioFUNC);
Our understanding of how NNTs, and non-native Á.B. by Plan Estatal I+D+i (Spain) and ESF through a
species in general, influence several ecosystem services pre-doctoral contract. Mateus Cardoso Silva helped with
simultaneously is poor (Vilà & Hulme, 2017). The approach data collection from Brazil. Megumi Uemura helped to
used here to identify associations among responses of extract information from Japanese documents. Our special
ecosystem services to NNTs represents a first crude gratitude to Elisabeth Pötzelsberger, chair of the Cost Action
exploration. Unfortunately, differences in scale of study FP1403 NNEXT, for all her support during the preparation
used for RES (species), and for PES, CES and EDS of this review.
(countries/regions), together with the limited number of
species or countries common to many ecosystem services, VII. AUTHOR CONTRIBUTIONS
precluded us from using a multivariate approach (Spake
et al., 2017). Such an approach would allow identifying P.C.-D. and O.G. produced the study idea; P.C.-D.,
bundles of services according to their response to NNTs A.S.V., O.G., J.S.S., M.V.L., A.A. and A.S. designed
(Raudsepp-Hearne, Peterson & Bennett, 2010), knowing how the research; all authors contributed to data collection;
the impact on such bundles changes in space (Spake et al., P.C.-D., A.S.V. and O.G. organized and analysed the data;
2017) and thus identifying areas most at risk from NNTs. P.C.-D. led the writing and A.S.V., O.G., J.S.S., M.V.L.,
D.M.R. and M.V. contributed to the first draft; all authors
contributed to the final version of the manuscript.
V. CONCLUSIONS
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Zanne, A. E., Tank, D. C., Cornwell, W. K., Eastman, J. M., Smith, S. A., Fig. S3. Funnel plots for each meta-analysis on the effect of
FitzJohn, R. G., McGlinn, D. J., O’Meara, B. C., Moles, A. T., Reich, P. B.,
Royer, D. L., Soltis, D. E., Stevens, P. F., Westoby, M., Wright, I. J., et al. non-native trees on regulating ecosystem services (RES).
(2014). Three keys to the radiation of angiosperms into freezing environments (vol Table S2. Analysis of publication bias in the meta-analyses
506, pg 89, 2014). Nature 514, 394–394. exploring the effects of non-native tree species on regulating
ecosystem services (RES).
Table S3. Comparison of meta-analysis models constructed
to assess the grand mean effect sizes of non-native tree (NNT)
species on regulating ecosystem services (RES).
IX. SUPPORTING INFORMATION Table S4. Heterogeneity (Q M ) of effect sizes of non-native
tree (NNT) species on regulating ecosystem services (RES)
Additional supporting information may be found online in across case studies explained by four qualitative predictors
the Supporting Information section at the end of the article. under random-effects structured meta-analysis.
Appendix S1. Sources of information used in each country Table S5. Results of the linear models relating the effect
to obtain the list of native and non-native tree species. size of non-native tree species on timber provision with five
Appendix S2. List of references identified by our search socio-economic and demographic predictors.
criteria for regulating ecosystem services. Table S6. Comparison of meta-analysis models constructed
Appendix S3. How we dealt with pseudo-replicates in to assess the grand mean effect size (and its 95% confidence
regulating ecosystem services. intervals, CI) of non-native tree (NNT) species on cultural
Appendix S4. Detailed protocols for statistical analysis. ecosystem services (CES) and on the disservice (EDS) pollen
Appendix S5. Description of data sources of provisioning allergenicity.
ecosystem services. Table S7. Structured meta-analysis assessing the contri-
Appendix S6. Description of data sources of cultural bution of predictors to explaining the heterogeneity of
ecosystem services and the disservice pollen allergenicity. non-native tree (NNT) species effect size on cultural ecosys-
Appendix S7. Description of data sources of predictors used tem services and on the disservice pollen allergenicity.
to explain the variation of the effects of non-native trees on Table S8. Effect size of non-native tree species on cultural
ecosystem services. ecosystem services (CES) and on one disservice (pollen
Fig. S1. Number of case studies on provisioning (PES), allergenicity), separated by biome.
cultural (CES), regulating services (RES) and ecosystem Table S9. Pairwise Spearman correlation coefficients among
disservice (EDS) per (sub)continent. the effects of non-native tree species on different regulating
Fig. S2. Number of case studies on provisioning (PES), ecosystem services.
cultural (CES), regulating services (RES) and ecosystem Table S10. Pairwise Spearman correlation coefficients
disservice (EDS) per biome. among the effects of non-native tree species on provisioning
Table S1. Non-native tree species in the regulating and cultural ecosystem services, and on the disservice pollen
ecosystem services (RES) data set. allergenicity.
(Received 16 March 2018; revised 13 March 2019; accepted 15 March 2019 )

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Biol. Rev. (2019), pp. 000–000.

Global effects of non-native tree species on

* Author for correspondence: (E-mail: Tel.: +34 91 8855091; mpilar.castro@uah.es).

(1) The data set . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

†Compound key words were introduced between inverted commas.

Values observed in the source associated

Climate Fire-risk Pollution Soil Soil Soil Water

(1) Our comprehensive worldwide review revealed more VIII. REFERENCES

(Received 16 March 2018; revised 13 March 2019; accepted 15 March 2019 )

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